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Open Access Research article

Independent specialisation of myosin II paralogues in muscle vs. non-muscle functions during early animal evolution: a ctenophore perspective

Cyrielle Dayraud1, Alexandre Alié12, Muriel Jager1, Patrick Chang3, Hervé Le Guyader1, Michaël Manuel1 and Eric Quéinnec14*

Author Affiliations

1 Université Pierre et Marie Curie - Paris 6, UMR 7138 CNRS MNHN IRD, Case 05, 4ème étage, Bâtiment A, 7 quai St Bernard, Paris 75005, France

2 Department of Biophysics, Laboratory of Molecular Developmental Biology, Graduate School of Science, Kyoto-University, Kitashirakawa-Oiwake, Sakyo-ku, Kyoto, 606-8502, Japan

3 Université Pierre et Marie Curie- Paris 6, UMR 7009 CNRS, Observatoire Océanologique, Villefranche-sur-Mer, 06230, France

4 UPMC Université Paris 6, UMR 7138 Systématique, Adaptation, Evolution CNRS MNHN IRD, Bâtiment A, 4ème étage, Case 05, Université Pierre et Marie Curie, 7 quai St Bernard, Paris 75005, France

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BMC Evolutionary Biology 2012, 12:107  doi:10.1186/1471-2148-12-107

Published: 2 July 2012

Abstract

Background

Myosin II (or Myosin Heavy Chain II, MHCII) is a family of molecular motors involved in the contractile activity of animal muscle cells but also in various other cellular processes in non-muscle cells. Previous phylogenetic analyses of bilaterian MHCII genes identified two main clades associated respectively with smooth/non-muscle cells (MHCIIa) and striated muscle cells (MHCIIb). Muscle cells are generally thought to have originated only once in ancient animal history, and decisive insights about their early evolution are expected to come from expression studies of Myosin II genes in the two non-bilaterian phyla that possess muscles, the Cnidaria and Ctenophora.

Results

We have uncovered three MHCII paralogues in the ctenophore species Pleurobrachia pileus. Phylogenetic analyses indicate that the MHCIIa / MHCIIb duplication is more ancient than the divergence between extant metazoan lineages. The ctenophore MHCIIa gene (PpiMHCIIa) has an expression pattern akin to that of "stem cell markers" (Piwi, Vasa…) and is expressed in proliferating cells. We identified two MHCIIb genes that originated from a ctenophore-specific duplication. PpiMHCIIb1 represents the exclusively muscular form of myosin II in ctenophore, while PpiMHCIIb2 is expressed in non-muscle cells of various types. In parallel, our phalloidin staining and TEM observations highlight the structural complexity of ctenophore musculature and emphasize the experimental interest of the ctenophore tentacle root, in which myogenesis is spatially ordered and strikingly similar to striated muscle formation in vertebrates.

Conclusion

MHCIIa expression in putative stem cells/proliferating cells probably represents an ancestral trait, while specific involvement of some MHCIIa genes in smooth muscle fibres is a uniquely derived feature of the vertebrates. That one ctenophore MHCIIb paralogue (PpiMHCIIb2) has retained MHCIIa-like expression features furthermore suggests that muscular expression of the other paralogue, PpiMHCIIb1, was the result of neofunctionalisation within the ctenophore lineage, making independent origin of ctenophore muscle cells a likely option.